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Characterization of Ectomesenchymal Cells Isolated from the First Branchial Arch During Multilineage Differentiation

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Characterization of Ectomesenchymal Cells Isolated from the First Branchial Arch During Multilineage Differentiation http://www.paper.edu.cn Original Paper Cells Tissues Organs 2006;183:123–132 Accepted after revision: July 18, 2006 DOI: 10.1159/000095986 Characterization of Ectomesenchymal Cells Isolated from the First Branchial Arch during Multilineage Differentiation a, b c b c d Zhengbin Yan Yunfeng Lin Xiaohui Jiao Zhiyong Li Ling Wu c c c c c c, d Wei Jing Ju Qiao Lei Liu Wei Tang Xiaohui Zheng Weidong Tian a b c Daqing Oilfields General Hospital, Daqing , Harbin Medical University, Harbin , Department of Oral and d Maxillofacial Surgery, West China College of Stomatology, and Key Laboratory of Oral Biomedical Engineering, Ministry of Education, Sichuan University, Chengdu , China Key Words The adipogenic ectomesenchymal cells showed accumula- Craniofacial development Stem cell differentiation tion of lipid vacuoles and expression of lipoprotein lipase and Mesenchymal stem cells Cranial neural crest cells peroxisome proliferator-activated receptor 2 . Following os- First branchial arch teoinduction, the fibroblast-like cells became cuboidal and formed mineralized nodules. In addition, the expression of mRNA encoding osteocalcin and osteopontin proved osteo- Abstract genesis at the molecular level. Chondrogenic lineage ex- Ectomesenchymal cells isolated from the first branchial arch pressed collagen type II, aggrecan and Sox9 with a low level have the potential to differentiate into a variety of cell lineag- of collagen type I in monolayer culture. Odontogenesis was es both in vitro and in vivo. This study was aimed to confirm determined by dentin sialophosphoprotein, collagen type I the plasticity of multilineage differentiation with molecular and dentin matrix protein 1 expression. Therefore, we have and cellular characterization. Monolayer cultures of ectomes- demonstrated that ectomesenchymal cells from the first enchymal cells harvested from the first branchial arch primor- dia in embryonic day 9.5 BALB/c mice were passaged 3 times before analysis. Staining with antibodies against S-100, p75 and vimentin suggested that the population of stem cells Abbreviations used in this paper originated from ectomesenchyme, with few contaminating cells stained for cytokeratin. Then, cells were transferred to BMSSCs bone marrow stromal stem cells CNCCs cranial neural crest cells adipogenic, osteogenic, chondrogenic and odontogenic me- Col-I collagen type I dia. The initiation of controlled differentiation was deter- Col-II collagen type II mined with histological assays, and the expression of tissue- DMP1 dentin matrix protein 1 specific genes was detected using immunocytochemical DSPP dentin sialophosphoprotein staining and reverse transcription polymerase chain reaction. ECM extracellular matrix OCN osteocalcin RT-PCR reverse transcription polymerase chain reaction Z.Y. and Y.L. contributed equally to this study. © 2006 S. Karger AG, Basel Dr. Weidong Tian 1422–6405/06/1833–0123$23.50/0 Department of Oral and Maxillofacial Surgery, West China College of Stomatology Fax +41 61 306 12 34 Sichuan University E-Mail [email protected] Accessible online at: Chengdu 610041 (China) www.karger.com www.karger.com/cto Tel. +86 28 8550 3406, Fax +86 28 8550 2117, E-Mail [email protected] 转载 中国科技论文在线 http://www.paper.edu.cn branchial arch are capable of extensive multilineage differen- Considerable progress has been made in recent years tiation in vitro, controllable by the culture environment. This in understanding the biology of pluripotent cells in the makes them a relevant and valuable source of stem cells for early embryo and how genetic and epigenetic mecha- research of craniofacial development and tissue engineering nisms mediate their subsequent lineage segregation, dif- of restoration. Copyright © 2006 S. Karger AG, Basel ferentiation and final contribution to a particular cell type [Soo et al., 2002; Tian et al., 2004]. Several studies have significantly advanced our understanding of migra- tion and development pathways of the ectomesenchymal Introduction cells during embryogenesis [Pasqualetti and Rijli, 2002; Cobourne and Sharpe, 2003]. However, the multilineage Cranial neural crest cells (CNCCs) contribute signifi- differentiation potential of these cells isolated from the cantly to the formation of craniofacial structures during first branchial arch has not yet been studied in detail, as embryonic development. CNCCs disperse from the dorsal they terminally differentiate to multiple phenotypes. surface of the neural tube and migrate extensively through Here, we report that ectomesenchymal cells can be in- the embryo, giving rise to a wide variety of differentiated duced to express multiple lineage-specific genes and pro- cell types [Stemple and Anderson, 1992; Jiang et al., 2005]. teins in differentiation-inducing culture systems sim- These cells migrate into the first branchial arch from the ilar to those used with bone marrow stromal stem cells midbrain and anterior hindbrain around the 4-somite (BMSSCs). These results confirm the multipotential dif- stage and are then termed ‘ectomesenchymal cells’ [Osu- ferentiation capability of these cells and show that it can mi-Yamashita et al., 1994; Yan et al., 2004]. be controlled by culture conditions. This will aid the elu- Ectomesenchymal cells from cranial neural crest mi- cidation of the mechanisms of craniofacial development, grate ventrolaterally as they populate the branchial arch- as well as point to avenues for stem cell manipulation that es during craniofacial development [Epperlein et al., may be useful in tissue engineering. 2000]. The proliferative activity of these cells produces the discrete swellings that demarcate each branchial arch. Postmigratory ectomesenchymal cells differentiate into Materials and Methods an array of phenotypes following the proper epithelial- Isolation and Culture of Ectomesenchymal Cells mesenchymal interaction and contribute to the forma- Eight-week-old BALB/c mice were used to generate embryos, tion of various head and neck structures [Garcia-Castro and embryonic day 0.5 was taken as noon of the day on which and Bronner-Fraser, 1999; Zhang et al., 2003]. They can vaginal plugs were detected. The first branchial arch primordia give rise to progeny including adipogenic, osteogenic, from embryonic day 9.5 mice were dissected under a microscope chondrogenic, neurogenic, myogenic and odontogenic ( fig. 1 A), minced and incubated in a 0.125% trypsin and 1-mmol/l EDTA solution for 5 min at 37 ° C with gentle agitation. The en- lineages, which form most of the oral and dental tissues zyme digestion was neutralized with fresh Dulbecco’s modified except the enamel organ [Chai et al., 2000; Christiansen Eagle’s medium (Gibco) containing 10% fetal bovine serum (Gib- et al., 2000; Sharpe, 2001]. The detailed morphogenesis co). Released cells were filtered and then collected by centrifuga- of ectomesenchymal structures (e.g., size, shape and tion at 1,000 g for 3 min. The pellet was resuspended, washed 3 2 number of teeth) is also determined by epithelial-mesen- times with medium and seeded on the 25-cm plastic culture f lasks (Corning Company, USA) in medium Dulbecco’s modified chymal interactions [Thesleff and Sharpe, 1997; Tucker Eagle’s medium/F12 (1: 1), containing 10% fetal bovine serum, and Sharpe, 1999]. 10 6 U/l leukemia inhibitor factor (Chemicon International, Te- Various growth factors (such as transforming growth mecula, Calif., USA), 100 U/ml penicillin and 100 g/ml strepto- factor- ) and transcription factors (such as Msx1 and mycin. After 20 min of incubation, most of the cells attached to Msx2) have been implicated in the specification, fate de- the flasks were ectomesenchymal cells, but fewer epithelial cells had attached due to their longer attachment time. The nonat- termination and pattern formation of ectomesenchymal tached cells were discarded, and fresh medium was transferred to cells [Chai et al., 1999; Semba et al., 2000; Takahashi et the flasks. Cells were maintained in a humidified atmosphere of al., 2001]. For instance, fibroblast growth factor 8, which 5% CO 2 at 37 ° C and passaged 3 times prior to specific induction is expressed in the anterior surface ectoderm of the first in different culture systems. arch, is essential for the polarity of the branchial arch Identification of Cultured Cells [Tucker et al., 1999; Irving and Mason, 2000]. Hence, Immunostaining with antibodies against vimentin (1: 50), S- many regulatory molecules play an important role in pat- 100 (1: 100; Dako Cytomation, Carpinteria, Calif., USA) and p75 terning the branchial arch derivatives. (1: 100; Boehringer Mannheim, Mannheim, Germany) was per- 124 Cells Tissues Organs 2006;183:123–132 Yan /Lin /Jiao /Li /Wu /Jing /Qiao /Liu / Tang /Zheng /Tian 中国科技论文在线 http://www.paper.edu.cn F i g . 1 . First branchial arch primordia un- der a microscope ( A). Primary cells showed a fibroblast-like morphology with 2–4 processes ( B). After 3 passages and expan- sion for 14 days, most of the cells were pos- itively immunostained with markers of undifferentiated ectomesenchymal and neural crest cells, including p75 ( C), vi- mentin ( D) and S-100 ( E). Few cells in the culture were labeled with antibody to cy- tokeratin ( F). Scale bar = 50 m. formed to identify the undifferentiated characters of primary ec- positive staining divided by the total number of cells counted and tomesenchymal cells. Contaminating dental epithelial cells were expressed as a percentage, was calculated. detected with antibody against cytokeratin (1: 100; Dako Cytoma- tion). The proportion
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